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Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Biol. Lett. (2011) 7, 168–172 inaccessible to the literate ability of 8- to doi:10.1098/rsbl.2010.1056 10-year-old children, and second, the true Published online 22 December 2010 motivation for any scientiﬁc study (at least one Animal behaviour of integrity) is one’s own curiousity, which for the children was not inspired by the scientiﬁc literature, but their own observations of theBlackawton bees world. This lack of historical, scientiﬁc context does not diminish the resulting data, scientiﬁcP. S. Blackawton1, S. Airzee1, A. Allen1, S. Baker1, methodology or merit of the discovery for the scientiﬁc and ‘non-scientiﬁc’ audience. On theA. Berrow1, C. Blair1, M. Churchill1, J. Coles1, R. F.- contrary, it reveals science in its truest (mostJ. Cumming1, L. Fraquelli1, C. Hackford1, A. Hinton naive) form, and in this way makes explicit theMellor1, M. Hutchcroft1, B. Ireland1, D. Jewsbury1, commonality between science, art and indeedA. Littlejohns1, G. M. Littlejohns1, M. Lotto1, all creative activities.J. McKeown1, A. O’Toole1, H. Richards1, Principal ﬁnding: ‘We discovered that bumble-L. Robbins-Davey1, S. Roblyn1, H. Rodwell-Lynn1, bees can use a combination of colour and spatialD. Schenck1, J. Springer1, A. Wishy1, relationships in deciding which colour of ﬂower to forage from. We also discovered that scienceT. Rodwell-Lynn1, D. Strudwick1 and R. B. Lotto2,*1 is cool and fun because you get to do stuff that Blackawton Primary School, Blackawton, Devon, UK no one has ever done before. (Children from2 Institute of Ophthalmology, University College London, Blackawton)’.11-43 Bath Street, London EC1V 9EL, UK*Author for correspondence (lotto@ucl.ac.uk). Keywords: Bombus terrestris; buff-tailed bumble-bee;Background: Real science has the potential to visual perception; colour vision; behaviournot only amaze, but also transform the wayone thinks of the world and oneself. This isbecause the process of science is little differentfrom the deeply resonant, natural processes of 1. INTRODUCTIONplay. Play enables humans (and other mam- (a) Once upon a time . . .mals) to discover (and create) relationships People think that humans are the smartest of animals,and patterns. When one adds rules to play, agame is created. This is science: the process of and most people do not think about other animals asplaying with rules that enables one to reveal being smart, or at least think that they are not aspreviously unseen patterns of relationships smart as humans. Knowing that other animals are asthat extend our collective understanding of smart as us means we can appreciate them more,nature and human nature. When thought of in which could also help us to help them.this way, science education becomes a more Scientists do experiments on monkeys, because theyenlightened and intuitive process of asking ques- are similar to man, but bees could actually be close totions and devising games to address those man too. We see bees in the natural habitat doing whatquestions. But, because the outcome of all they do, but you do not really see them doing humangame-playing is unpredictable, supporting this things—such as solving human puzzles like Sudoku.‘messyness’, which is the engine of science, is So it makes you wonder if they could solve a humancritical to good science education (and indeedcreative education generally). Indeed, we have puzzle. If they could solve it, it would mean that theylearned that doing ‘real’ science in public are really smart, smarter than we thought before,spaces can stimulate tremendous interest in which would mean that humans might have somechildren and adults in understanding the pro- link with bees. If bees are like us in some way, thencesses by which we make sense of the world. understanding them could help us understandThe present study (on the vision of bumble- ourselves better.bees) goes even further, since it was not only To get ready to do the experiments with the bees weperformed outside my laboratory (in a Norman ﬁrst talked about science being about playing gameschurch in the southwest of England), but the and making puzzles. We then got into groups and‘games’ were themselves devised in collabor- made up games to play using random pieces of physicalation with 25 8- to 10-year-old children. Theyasked the questions, hypothesized the answers, education equipment. This gave us experience ofdesigned the games (in other words, the exper- thinking of games and puzzles. We then had to explainiments) to test these hypotheses and analysed our games to other people. After talking about what itthe data. They also drew the ﬁgures (in coloured is like to create games and how games have rules, wepencil) and wrote the paper. Their headteacher talked about seeing the world in different ways by(Dave Strudwick) and I devised the educational wearing bug eyes, mirrors and rolled-up books. Weprogramme (we call ‘i,scientist’), and I trained then watched the David Letterman videos of ‘Stupidthe bees and transcribed the childrens’ words Dog Tricks’, in which dogs were trained to do funnyinto text (which was done with smaller groups things. Next, we too had to learn to solve a puzzleof children at the school’s local village pub). So that Beau (a neuroscientist) and Mr Strudwick (ourwhat follows is a novel study (scientiﬁcally and headteacher) gave us (which took an artiﬁcial brainconceptually) in ‘kids speak’ without referencesto past literature, which is a challenge. Although 10 000 trials to solve, but only four for us). Afterwards,the historical context of any study is of course we started asking questions about bees, and then moreimportant, including references in this instance speciﬁc questions about seeing colour using the beewould be disingenuous for two reasons. First, arena (ﬁgure 1).given the way scientiﬁc data are naturally We came up with lots of questions, but the one wereported, the relevant information is simply decided to look at was whether bees could learn toReceived 8 November 2010Accepted 30 November 2010 168 This journal is q 2010 The Royal Society

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Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Colour and spatial relationships in bees P. S. Blackawton et al. 169 (a) to remember the ﬂowers that were around it, which is like a puzzle. To test this we gave the bees a series of challenges to see if they could complete them or not, and then tested them to see if they solved the puzzle and how they solved it. It was a difﬁcult puzzle, because the bees could not just learn to go to the colour of the ﬂower. Instead, they had to learn to go to one colour (blue) if it was surrounded by the opposite colour (yellow), but also to go to the opposite colour (yellow) if it was surrounded by blue. We also wanted to know if all the bees solved the puzzle in the same way. If not, it would mean that bees have personality (if a bee goes to the blue ﬂower every time, it tells us that it really likes blue). 2. MATERIAL AND METHODS (b) (a) The bee arena The bee arena, which was made out of Plexiglas, had six sides. The arena was 1 m high, 1 m wide and 1 m deep, and two of the side panels had three doors each. It had a vertical lightbox at the end opposite the side through which the bees entered by a small hole. The lightbox was made out of aluminium, with a Plexiglas screen in front of the six ﬂuorescent lights. An aluminium cross was placed in front of the Plexiglas screen, and this cross had grooves in its sides so that we could slide four black aluminium panels into the cross. Each panel had 16 cut-out circular holes in four rows of four circles each. Each circle was 8 cm in diameter. The holes were covered by the Plexiglas screen. In the centre of each circle was a Plexiglas rod with a small hole in the middle in which we put sugar water, salt water or nothing. Behind each hole there were slits so that squares of coloured gel ﬁlters could be slotted in, making the light shining through each hole coloured. It was like put- ting a piece of coloured see-through paper on a light to let the colour of the paper shine through. (b) The bees The bees had black and yellow stripes with white bottoms. The type of bee was Bombus terrestris. The beehive was delivered from (c) Koppert (UK). (c) Training phase 1 To teach the bees to go to the Plexiglas rods as if they were ﬂowers, all the circles in every panel were kept white, and all the rods had sugar water in them. Once the labelled foragers learned that the ﬂowers contained a reward, which took four days, we marked the bees, and then set up the puzzle. (d) Marking bees We let the foragers into the arena and turned the lights off, which made the bees stop ﬂying (because they do not want to ﬂy into any- thing). We picked the bees up with bee tweezers and put them into a pot with a lid. We then put the tube with the bees in it into the school’s fridge (and made bee pie ). The bees fell asleep. Once they fell asleep, we took the bees out, one at a time, and painted little dots on them (yellow, blue, orange, blue-orange, blue-yellow,Figure 1. Conditions and responses to ‘test 1’ (control). etc.). We put them into the tube and warmed them up and then(a) The pattern of colours that the bees were trained to let them into the arena. No bees were harmed during this procedure.and tested on in their ﬁrst test (see text for explanation).(b) The selections made by all the bees tested (dots show (e) Training phase 2 (‘the puzzle’ . . .duh duh duuuuhhh)where each bee landed and tried to get sugar water). (c) A We set up a puzzle for the bees as in the following. Imagine having atable showing the preferences of each bee during testing panel with 16 circles, with a large square of 12 yellow circles on the outside and a small square of four blue circles in the middle. This(see text for explanation). was the case for two panels, but the other two panels were the oppo- site, and instead of yellow on the outside as the larger square and blue on the inside as the smaller square, we had blue on the outsideuse the spatial relationships between colours to ﬁgure and yellow on the inside. The sugar reward (1 : 1 with water) wasout which ﬂowers had sugar water in them and only in the middle four ﬂowers inside each panel of 16 ﬂowers. Every 10 –40 min, we swapped the locations of the panels aroundwhich had salt water in them. It is interesting to ask the different quadrants so that the bees could not learn the locationsthis question, because in their habitat there may be of the rewarding ﬂowers. We also cleaned the Plexiglas stems so thatﬂowers that are bad for them, or ﬂowers from which the bees could not use scent to tell the other bees that ﬂower had thethey might already have collected nectar. This would reward. Instead they had to learn: if there was blue on the outside ring of each panel of 16 circles, then they had to go to the innermean that it is important for bees to learn which four yellow circles. If, however, there was yellow on the outsideﬂower to go to or to avoid, which would need them ring, then they had to go to the inner four blue circles. During theBiol. Lett. (2011)

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Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012170 P. S. Blackawton et al. Colour and spatial relationships in beesﬁrst 2 days of training, sugar water was placed only in the four middle (a)ﬂowers in each panel and nothing in the outside ring (so that theywould get the hang of it). During the second 2 days we added saltwater to the ﬂowers in the outside rings. We did this so that theywould learn not to go just to the colours, but had to learn the pattern.Otherwise they might fail the test, and it would be a disaster. Aftertraining, we tested the bees to see if they solved the puzzle.(f) Testing the beesWe tested the bees using the same pattern of colours, but withoutsugar water or salt water, to see which ﬂowers they would go to.We also moved the locations of the panels so that the layout wasdifferent from when they were just trained. We let the labelled for-agers into the arena one at a time so that they would not copyeach other (as humans might). We tracked their ﬂower choicesusing a sheet of paper with the 64 circles marked into the four quad-rants. Whenever the bees landed on a ﬂower and stuck their tongue(proboscis) into the Plexiglas rod, we would mark the matching circleon the sheet. We marked each circle with a ‘1’, a ‘2’ or a ‘3’ and soon, to track where they went to see how their behaviour might havechanged with time. After a while, the bees might have got annoyedbecause they were not getting a reward, and might have startedmaking mistakes or searching randomly. So we let each foragermake only around 30 choices before stopping the test. Each bee (b)was tested three times (see §3).3. RESULTSAfter training the bees in the arena, we tested themthree times to see if they had learned anything duringtraining.(a) Test 1 (the control)In the ﬁrst test the bees were given the same pattern wehad trained them with. After training, we moved thecolours of the panels clockwise once, so that the col-ours of the quadrants would be different for the bees,and they could not just go to the same place as lasttime to get a reward (see ﬁgure 1a for a hand drawing Figure 2. Conditions and responses to ‘test 2’. (a) The pat-of the test). If the bees had solved the puzzle, they tern of colours that the bees were tested on in their secondshould land on the ﬂowers in the middle of each quad- test (see text for explanation). (b) A table showing the prefer-rant and stick their tongues (proboscis) in the ﬂower, ences of each bee during test 2 (see text for explanation).as during training this is how they would have had areward (during the test, they did not get a reward). Figure 1b shows where four of the bees went during went to 31 correct yellow ﬂowers and four incorrectthe test (unfortunately, one of the bees (called ‘yellow’) yellow ﬂowers, and never went to blue ﬂowers. Thedid not come out of the hive during this test). Each dot ‘Blue’ (B) bee went to 33 correct yellow ﬂowers andin ﬁgure 1b is an attempted forage. The ﬁgure shows only three incorrect yellow ﬂowers, and selected thethat the bees went to the middle ﬂowers 126 times, correct blue ﬂowers only once. These results areand to the outside ﬂowers in the four quadrants a shown in ﬁgure 1c. We conclude that one bee wenttotal of 13 times (see ‘total’ in ﬁgure 1c). So, out of to a mixture of colours in the correct locations, but139 attempted forages, 90.6 per cent were to correct the rest preferred one colour over the other. However,ﬂowers (correct means ﬂowers that would have had although they preferred one colour, they only went tosugar water during training). the middle of the panel that had that colour (as this Figure 1c shows how many times each individual bee is the ﬂower that would have had a reward). This testwent to correct and incorrect blue and yellow ﬂowers. shows that altogether the bees solved the puzzle veryWe did this so that it would be clearer to see where well, as their choices collectively were divided betweeneach bee went during the test. ‘Orange’ (O) bee all blue and yellow rewarding ﬂowers. We then pre-selected seven correct (middle) yellows and only one sented the bees with two more tests to see how theyincorrect (outside) yellow. She also went to 29 correct solved the puzzle they were trained for.blue and only one incorrect blue. This bee prefers bluein the middle, but also prefers yellow in the middle. (b) Test 2 (the ﬁrst experiment)This bee did extremely well, because it went to Test 2 was very similar to test 1, except that the middleboth colours at correct locations in the ﬂowers. ﬂowers in each quadrant were green. We did this to see‘Blue/yellow’ (B/Y) bee went to neither outside whether the bees learned to go to the colours or to theyellow ﬂowers nor middle yellow ﬂowers. Instead it location of the rewarding ﬂowers during training. If thewent to 25 correct blue ﬂowers (middle) and only bees learned to go to the location of the rewardingfour incorrect blue ﬂowers (outside). So this bee pre- ﬂowers, then they should land on the green ﬂowers inferred blue to yellow. The ‘Blue/Orange’ (B/O) bee test 2. See ﬁgure 2a for a hand drawing of this test.Biol. Lett. (2011)

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Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Colour and spatial relationships in bees P. S. Blackawton et al. 171 (a) ﬂowers. If the bees had learned to go to ﬂowers that were fewest in each panel, then they should go to the ﬂowers in the corners. The table in ﬁgure 3b shows where all ﬁve bees went during the test. You can see that the bees as a group went to the corner ﬂowers 59 times, and to the ‘not- corners’ 86 times (see ‘total’ in ﬁgure 3b). So, out of 145 attempted forages, 40.1 per cent were to the corners. This is very different from what they did in test 1. When the same ﬂowers were not in the corners but in the middle as in test 1, they selected them 90.6 per cent of the time, which is 2.2 times more often. We think that the bees in test 3 selected the ﬂowers randomly, and conclude that the bees did not learn to go to the ﬂow- ers that had the fewest colours in each panel. Also, this time, the B and B/O bees did not prefer the middle ﬂow- ers in each panel. This means that in test 2 they must have used the larger square of blue and yellow ﬂowers to decide to forage from the middle green ﬂowers. (b) 4. DISCUSSION This experiment is important, because, as far as we know, no one in history (including adults) has done this experiment before. It tells us that bees can learn to solve puzzles (and if we are lucky we will be able to get them to do Sudoku in a couple of years’ time). In this experiment, we trained bees to solve a particular puzzle. The puzzle was go to blue if surrounded by yellow, but yellow if surrounded by blue. Test 1 showed that the bees learned to solve this puzzle. We know this because the test results showedFigure 3. Conditions and responses to ‘test 3’. (a) The pattern that they mostly went to the ﬂowers that they were sup-of colours that the bees were tested on in their third test (see posed to go to, because those were the ones that hadtext for explanation). (b) A table showing the preferences of contained a sugar reward before. However, we alsoeach bee during test 3 (see text for explanation). noticed that the bees solved the puzzle in different ways, and that some were more clever than others. Two bees preferred yellow and two others preferred Figure 2b shows a table of the choices made by the blue ﬂowers. The B bee was best at understandingbees during this test. In total, the bees went to the the pattern in the ﬁrst test, because it had the most cor-green middle ﬂowers only 34 times, and to the outside rect answers compared to incorrect answers. It alsoblue and yellow ﬂowers 76 times (see total in went both to correct yellow and correct blue ﬂowers,ﬁgure 2b). So, out of 110 attempted forages, 30.9 per although it preferred the blue ﬂowers.cent were to the middle ﬂowers. If the bees were gues- What is important about this puzzle is that there issing, they should have selected the green ﬂowers 25 per more than one strategy the bees could use to solve it.cent of the time, which is very close to 30 per cent. So One strategy would be to use two rules: (i) go to thewe conclude that the bees did not solve test 1 by only middle four ﬂowers in each panel, and (ii) ignore thegoing to the middle ﬂowers of each quadrant (‘dah colour. Another strategy would be to go to yellow ifdahhh dahhhhhh’). However, two of the bees (labelled surrounded by blue or blue if surrounded by yellow.B/O and B) went most often to the green, middle They could also learn to avoid the surrounding ﬂowers,ﬂowers. So they seemed to have learned a different and as a result only go to the middle ﬂowers. Or theyrule to the other three bees. could go to the fewest number of coloured ﬂowers in each panel. Of course they could also have chosen(c) Test 3 (the second experiment) randomly, and they might get them right or theyIn the third test, instead of having large squares of might get them wrong. Or they could have just goneyellow and blue around the outside of each panel, to a colour, but then they would not have solved theand a smaller square of yellow and blue on the inside whole puzzle, only half of it.of each panel, we took the four inside ﬂowers and Test 2 tested whether the bees had learned to go toput them in the corners of each panel. See ﬁgure 3a the middle of each panel and ignored the colour. If thisfor a hand drawing of what this test looked like. We was true then they should have gone to the green ﬂow-did this because we wanted to see if the bees solved ers. If they had learned to go to only middle blue andtest 1 by learning during training to go to the colours yellow ﬂowers, then they should have gone either to theof each panel that were fewest in number. We could surrounding blue and yellow ﬂowers or no ﬂowers atalso see if they still preferred to go only to the middle all. The results tell us that three of the bees preferredBiol. Lett. (2011)

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Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012172 P. S. Blackawton et al. Colour and spatial relationships in beesto go to the colours that they had learned before, and Before doing these experiments we did not reallyavoided the middle green ﬂowers. Two of the bees, think a lot about bees and how they are as smart ashowever, mainly went to the middle ﬂowers, including us. We also did not think about the fact that withoutthe B bee, which went to both correct yellow and cor- bees we would not survive, because bees keep the ﬂow-rect blue ﬂowers during the ﬁrst (control) test. So they ers going. So it is important to understand bees. Wehad learned to solve the puzzle using different rules. discovered how fun it was to train bees. This is alsoTest 3 also showed that one of the rules was not just cool because you do not get to train bees everyday. Weto go to any middle ﬂower, as they rarely went to the like bees. Science is cool and fun because you get to domiddle ﬂowers, or to go to the ﬂowers that had the stuff that no one has ever done before. (Bees—seemfewest colours in each panel, because they did not to—think!)prefer the corner ﬂowers. Instead, they seemed toselect the ﬂowers at random, but funnily continued We thank the whole of the Blackawton community, who trulyto go to their ‘favourite’ colour. engaged with the science research, including the George We conclude that bees can solve puzzles by learning Inn—where the manuscript was written—for the free Cokescomplex rules, but sometimes they make mistakes. for the children (and pints for others). We thank the localThey can also work together (indirectly) to solve a parish for the use of the Norman church, where the experiments were run, and the parents for letting theirpuzzle. Which means that bees have personality and children ‘work’ outside ‘normal’ school hours. Of coursehave their personal ‘likings’. We also learned that the none of this would have happened without the innovativebees could use the ‘shape’ of the different patterns of indi- and enthusiastic support of the teachers of Blackawton. Wevidual ﬂowers to decide which ﬂowers to go to. So they are are also indebted to Larry Maloney and Natalie Hempel dequite clever, because they can memorize a pattern. This Ibarra for their openness to possibility and time, effort andmight help them get more pollen from ﬂowers by learning detail in writing the commentary, as well as Dale Purves,which ﬂowers might be best for them without wasting Lars Chittka, Read Montague, Karl Friston and Geoff North (Current Biology) for their sage advice. Finally, weenergy. In real life this might mean that they collect infor- thank Chris Frith and Brian Charlesworth for their open-mation and remember that information when going into mindedness. The project was funded privately by Lottolabdifferent ﬁelds. So if some plants die out, they can learn to Studio, as the referees argued that young people cannot doﬁnd nectar in another type of ﬂower. real science.Biol. Lett. (2011)